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Prevalence of Helicobacter pylori Infection in Arak, during 2011 Ali Fani1, Mohammad Rezaei2, Behruz Alizade1, Parisa Mirzajani1, Soheila Shamsikhani3, Mohammad Rafeie1, Ali Akbar Malekirad4, Saeed Baghi Nejad5 Original Article 1 Arak University of Medical Sciences, Arak, Iran 2 Department of Food Safety and Hygiene, School of Public Health, University of Medical Sciences, Tehran, Iran 3 Faculty of Midwifery and Nursing, Arak University of Medical Sciences, Arak, Iran 4 Payame Noor University, Tehran, Iran 5 Amiralmomenin Hospital, Arak University of Medical Sciences, Arak, Iran ABSTRACT

Background: Helicobacter pylori (H. pylori) is a global pathogen with a widely varied prevalence (30%-80%) among different countries and populations. This study aims to determine the prevalence of H. pylori in the population of Arak, Iran. Materials and Methods: This was an epidemiologic cross-sectional population-based study with multistage sampling. The population of $UDNDFFRUGLQJWRWKHFHQVXVZDV XUEDQDQGUXUDOUHVLGHQWV ,QWKLVVXUYH\¿YH urban and four rural Health Service Centers were randomly selected. The study population was divided between these centers based on the population of individuals covered by these centers. Subsequently, clustered samples were randomly chosen according to Health Care Unit Family Codes and the Right Hand Rule. After obtaining informed consent and completion of a demographic questionnaire, 5 cc of venous blood was taken from each participant for the H. pylori IgG antibody test. In this study IgG antibody against H. pylori was measured by ELISA. Results: Of 1187 participants, 1150 (853 urban and 297 rural) completed the study. Overall, 673 (58.5%) were positive for H. pylori. The prevalence of H. pylori infection increased with age from 43.9% among those <20 years old to >70% in participants over 50 years old (p=0.002). A total of 57% urban samples and 63.3% rural samples were H. pylori pos- itive (p=0.028). There was no relationship between H. pylori infection and education level (p=0.37), career (p=0.39) and income, (p=0.29) in either the urban or rural areas [p=0.64 (education level), 0.48 (career), and 0.57 (income)]. Conclusion: Our study showed a lower prevalence of H. pylori compared to some Asian countries, however this prevalence was more common than Western countries. Using disinfected tap water in both urban and rural areas in addition to improved access to general health care might have a role in this relative lower prevalence. Keywords: Prevalence; Helicobacter pylori; Infection; ELISA; Arak, Iran

please cite this paper as: Fani A, Rezaei M, Alizade B, Mirzajani P, Shamsikhani S, Rafeie Mohammad, Malekirad AA, Baghi Nejad S. Prevalence of Helicobacter pylori Infection in Arak, Iran during 2011. Govaresh 2014;19:57-62.

Corresponding author: INTRODUCTION Helicobacter pylori (H. pylori  ZDV ¿UVW Ali Fani, MD described by Warren and Marshall(1). H. pylori is Arak University of Medical Sciences, Arak, Iran a major cause of gastritis and peptic ulcer disease Tel: +98 918 1617447 (PUD) and has been implicated in the development E-mail: [email protected] of gastric malignancies and common worldwide Received: 20 Jan. 2014 infections (2-6). Previous sero-epidemiologic studies Edited: 28 Feb. 2014 have estimated that approximately 50% of adults Accepted: 29 Feb. 2014 worldwide, 20%-30% in developed countries and up to 80% in developing countries are positive for serum

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antibodies against H. pylori WGO 2010(5). The prevalence of H. pylori infection in the general adult prevalence is declining in most developed countries population of Arak, Markazi Province, Iran. (4,6,7). Epidemiological studies have shown that infection is mainly acquired in early childhood and MATERIALS AND METHODS the incidence increases with age (8-10). Close contact, This cross-sectional epidemiologic population- low socioeconomic status and poor hygiene are the EDVHGVWXG\ZDVFRQGXFWHGGXULQJD¿YHPRQWKSHULRG most important risk factors (5,10,11). It seems that the from March to July 2011 to determine the prevalence of fecal-oral route is the main basis of the infection (11- H. pylori infection on people over the age of 20 years in 13). Primary acquisition in adults or reinfection after Arak, Markazi Province, Iran. The population of Arak successful eradication does occur but is less common according to the 2006 census was 615,702 (493,845 with an annual incidence of 0.3%- 0.7% in developed urban and 181,857 rural). This study recruited 1150 countries and 6%-14% in developing countries (5, participants based upon a sample size that took into 11). Since humans are the main known reservoir for consideration the world wide prevalence (4) of 20%- infection, it is likely that in developed countries H. 80%, p G DQGĮ DQGZDVHVWLPDWHGDW pylori is acquired predominantly via the oral-oral and 1150 (853 urban, 297 rural) individuals who represented fecal-oral routes (11-13). Since the acute acquisition the general population based on the weighted multistage of H. pylori infection usually remains undiagnosed, VWUDWL¿HGFOXVWHUSDWWHUQIRUVDPSOLQJ$OOLQGLYLGXDOV the incidence has been determined indirectly through over the age of 15 years were enrolled with respect epidemiological studies. Some discrepancies between to the urban-rural population distribution. The Arak the prevalence and incidence data may be explained Township Health Service is covered by 11 urban and by the decreasing rates of infection over time. Thus, 8 rural Health Service Centers. In this survey 5 urban adults who are currently infected are more likely to and 4 rural Health Service Centers were randomly have acquired their disease in childhood rather than selected. The study participants were divided between during adulthood (2-5,14). these centers based on the population covered by Water has been suggested as a possible source of H. these centers. Subsequently, the clustered sample was pylori infection (15-24). Studies by Dube in Africa(25), randomly chosen according to the Health Care Unit Shi et al (26), and Kelin in Peru(14), Hopkin in Chile Family Codes and Right Hand Rule. After obtaining (27) have found that the water source may be related to informed consent and completion of the demographic the risk of H. pylori infection. One of the most important questionnaire that included items such as gender, age, factors increases risks of H. pylori infection in children, height, weight, education level, family member, career drinking water from a stream that may be vulnerable and family income, a total of 5 cc of venous blood to bacterial contamination. Studies have also assessed was taken from each participant for the H. pylori IgG the relation between H. pylori infection and various antibody test. Serum was directly separated and stored hygiene practice indicators in a number of countries. DW ஈ& ,Q FDVH RI WKH SDUWLFLSDQW UHIXVHV VDPSOHV Poor hygiene practices, especially during childhood, were collected from the nearest neighbor. H. pylori appear to be related to a higher sero-prevalence of status of the samples was determined by the ELISA IgG H. pylori. Some practices include the lack of a water Antibody Mono-bind Inc. H. pylori Kit (no CA92630, closet or bathroom or no hot water supply in the house USA) and by a Stat Fax 3200 (USA) ELISA reader during childhood, sharing cups as children, and having WKDWKDGDVHQVLWLYLW\RIDQGVSHFL¿FLW\RI mothers who did not use soap when they washed their Any titer above 20 units was considered positive. Data hands (20,27-29). Although there are different tests for were analyzed with SPSS version 11.5, the chi-square the detection of H. pylori, the ELISA method remains test, logistic regression and t-test. p-values <0.05 were a reliable and cost effectiveness test for epidemiologic FRQVLGHUHGVWDWLVWLFDOO\VLJQL¿FDQW studies (5,30). Public knowledge and expectations have also increased, with numerous patients requesting RESULT information about the chances of acquiring the From 1187 participants, 1150 participants (853 urban infection, risk of peptic ulcer, gastric cancer and routes and 297 rural) completed the study. Participants' mean of transmission. In order to provide accurate answers, it age was 39.22±12.7 years. Overall, 673 (58.5%) had LVQHFHVVDU\WRFRQGXFWHSLGHPLRORJLFDOVWXGLHVVSHFL¿F evidence of antibodies to H. pylori (ELISA IgG- Ab+); to areas of interest and update data with improvement 57% urban and 63% rural samples were antibody positive. of health level. This study intends to determine the According to two-tailed analysis, there was no difference

58 Govaresh/ Vol.19/ No.1/ Spring 2014 H. pylori Infection in Arak

in the positive H. pylori results between urban and rural QRWVLJQL¿FDQW$VWXG\LQ6KLUD]  UHSRUWHGH. populations (p=0.379). However in the one-tailed test, pyloriSRVLWLYLW\$OWKRXJKWKHLU¿QGLQJVZHUHVLPLODUWR this overall difference was meaningful (p=0.038). The WKH¿QGLQJVRIWKHFXUUHQWVWXG\WKHVHUHVXOWVPLJKWQRW prevalence of H. pylori infection increased with age from be comparable because subjects in the study were 43.9% among <20 year-old group to >70% in those over selected from patients with dyspepsia who had higher 50 years of age (p=0.002). There was no relationship rates of current infection and were not representative between H. pylori infection and education level (p=0.37), of the general population. Results of these studies have career (p=0.35) and income (p=0.29) for urban residents, shown that the prevalence of H. pylori infection in Iran or for rural residents in terms of education level (p=0.64), varies according to ethnicity, cultural and healthcare career (p=0.48), and income (p=0.57). Regarding gender, factors. The overall prevalence of H. pylori infection in 57% of women and 60.08% of men were H. pylori positive our study was lower than some published studies from ZKLFKZDVQRWVLJQL¿FDQW S  $PRQJPDOHV other developing countries (22, 32). In comparison with of urban and 62.1% of rural groups were seropositive Asian countries such as Kazakhstan, Bangladesh and (p=0.092). In females, 54.7% of urban and 64.8% of rural , we have shown that H. pylori infection was less groups were seropositive (p=0.028). Average BMI in the common in Iran (Arak) and inversely correlated with the H. pylori negative group was 25.03±4.55 whereas in the health care system and more common use of closed wells H. pylori positive group it was 25.94±16.14 (p=0.238). DQGKRWZDWHU)DPLO\FURZGLQJVKRZHGQRVLJQL¿FDQW Heartburn symptoms were seen in 11.3% of seronegative effect on H. pylori prevalence in Iran and Kazakhstan and 16.9% of seropositive participants (p=0.207). In Arak, (15). H. pylori infection appeared to be less common all study participants in both urban and rural areas used in Iran compared to other Middle Eastern countries. An chlorinated closed well water. overall estimation of H. pylori prevalence in Turkey was 82.5% according to the Urea Breath Test (UBT) method DISCUSSION as reported by Sinan (31). Although comparable with We used epidemiologic study data to produce the some Iranian studies, there was a meaningful difference population-based estimation of the prevalence of H. with the results of the current study (p=0.001). In a review pylori infection in Arak and explored the relationships article from Africa(25), the prevalence of H. pylori between various demographic factors of infection. infection was reported to be 74.8%-92% and depended 7KHUH ZDV QR VLJQL¿FDQW GLIIHUHQFH LQ WKH SUHYDOHQFH on the drinking water source (tap water versus well of H. pylori between the urban and rural population water) which was more common than Iran, particularly (p=0.379). The lower rate of infection in the urban Arak. Tkachenko et al. (22) in a 10-year follow-up population could be related to improvements in public VWXG\LQ5XVVLDREVHUYHGDVLJQL¿FDQWGURSIURP health care services (availability of hot water and soap in 1995 to 25% in 2005 in H. pylori infection among use). In this study, in terms of gender we observed no 15-19 year olds which was concurrent with health care difference in the prevalence of H. pylori in both the rural improvements. They concluded that there was an inverse and urban areas. However this prevalence was slightly correlation between mothers' and fathers' educational more common in females from rural areas compared levels and H. pylori sero-positivity. In our study there to urban females, which might be related to the family was no association between the prevalence of H. pylori crowding and poorer hygienic conditions in rural areas. and any factor tested, including sex, type of dwelling, Few epidemiologic and community-based studies income, or the number of people living in the home. that determined the H. pylori infection in the general These results were inversely comparable with the same population have been performed in Iran. The majority DJHJURXS¿QGLQJVLQD5XVVLDQVWXG\ p=0.017) (22). of these studies were undertaken in gastroenterology Naja et al. (8), conducted a sero-epidemiologic study in clinics (16,24,30). Overall, our survey results showed , Canada among individuals 50 to 80 years of lower prevalence than previous epidemiologic age. In that study a prevalence of 23.1% with a higher studies conducted in (67.1%) prevalence among males was reported. The sample size and Nahavand 71% (16,19). In the <20 year old age and methods were similar to the current study, however group, we reported a prevalence of 43.9%, which was the age factor differed. Staat et al. (23) studied H. more common than the prevalence in that had a pylori infection in the US population by measuring IgG 30.6% H. pylori sero-positivity (p=0.045) (18). This antibody levels in serum from 2581 subjects aged 6-19 GLIIHUHQFHZDVVLJQL¿FDQW,QFRPSDULVRQZLWK$UGDELO years. Overall, 24.8% of participants had evidence of that reported a 47.5% sero-positivity, the difference was H. pylori infection which was less common than our

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Table 1: World Gastroenterology Organization Global Guidelines for Helicobacter pylori (H. pylori) in developing and developed countries, August 2010. Developing Countries H. pylori positive Developed Countries H. pylori positive Country Age group <20 years Adults Country Age group <20 years Adults

Africa - - North America

Ethiopia <6 80% 95% Canada <20 7.1% 50-80 23.1% Nigeria <10 82% 91% USA and Canada - 30% Central & South - - Hong Kong <20 13.1% - America Guatemala <10 51% 70-90% Japan - 20-70 55.4% Mexico <10 43% 70-90% Taiwan 13–15 12.3% >25 45.1% Brazil 10-19 78% 82% Australasia <20 15.4% 20%

Chile <10 36% 70-90% Europe -

Asia - - Eastern Europe - 70% Bangladesh <10 82% 90% Eastern Europe - 30-50% India <20 87% 88% Germany - 48.8%

Turkey General population 82.5% Iceland 36%

Table 2: Summary and prevalence comparison of H. pylori in residents <20 years of age from Arak, Iran with studies in Iran and other countries. Method, sample size, results Country Editor, year published Study population (years) Sample size and p-value Negative Positive method Iran, Arak Present study, 2011 <20 66 ELISA 37 (56.06%) 29 (43.94%) Iran, Mikaeili(18), 1999 <20 358 ELISA 188 (52.5%) 170 (47.5%) 0.688 Iran, Yazd Mikaeili(18), 1999 <20 353 ELISA 245 (59.4%) 108 (30.6%) 0.045 Turkey Apan(20), 2008 <20 529 ELISA 370 (70%) 159 (30%) 0.025 Russia Tkachenko(22), 2005 15-19 100 ELISA 75 (75%) 25 (25%) 0.017 Kazakhstan Nurgalieva(15), 2002 15-19 55 ELISA 20 (36%) 35 (64%) 0.044

Table 3: Summary and prevalence comparison of H. pylori in Arak, Iran with studies held in Iran and other countries (general population). Method, sample size, results Country Editor, year published Population selection Sample size and p-value Negative Positive method

Iran, Arak Present study, 2011 General population 1150 ELISA 477 (41.5%) 673 (58.5%)

Iran, Hormozgan Hashemi(16), 2006 Adult dyspeptic 1000 RUT1 329 (32.9%) 671 (67.1%) 0.001 Turkey Sinan(31), 2009 General population 2382 ELISA 82.5% 0.001 Iran, Nahavand Alizadeh(19), 2009 General population 1518 ELISA 449 (29%) 1078 (71%) 0.001 India Klein(14), 1991 General population 238 ELISA 50 (17.5%) 188 (79%) 0.001 Canada, Toronto Naja(8), 2007 50-80 years 1306 ELISA 922 (70.6%) 384 (29.4%) 0.001

1Rapid urease test

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Table 4: Comparison of H. pylori sero-positive age groups in urban and rural populations of Arak, Iran during 2011. Urban Rural Age group (years) p-value Samples (n) Seropositive n (%) Samples (n) Seropositive n (%) <20 35 14 (40) 31 15 (48.4) 0.824 21-30 219 153 (61.2) 62 32 (51.6) 0.902 31-40 250 153 (61.2) 85 58 (69.4) 0.901 41-50 186 112 (60.2) 55 35 (63.6) 0.901 51-60 115 66 (57.4) 45 32 (71.1) 0.484 61-70 40 24 (60) 19 15 (73.7) 0.665 >70 8 7 (87.5) 0 0 - Sum 853 486 (57) 297 187 (63) 0.379

Table5: The relationship between H. pylori and family income (toumans/month/ person) Low income (<100000) Moderate income (200000-400000) High income (>400000) p-value H. pylori negative 137 (28.7%) 328 (68.8%) 12 (2.5%) 0.209

H. pylori positive 215 (32%) 453 (67.3%) 5 (0.7%)

Total 352 (30.6%) 781 (67.9%) 17 (1.5%)

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